Abstract
In the transition zone between aquifers and basal aquitards, the perchloroethene pools at an early time in their evolution are more recalcitrant than those elsewhere in the aquifer. The aim of this study is to demonstrate that the biodegradation of chloroethenes from aged pools (i.e., pools after decades of continuous groundwater flushing and dissolution) of perchloroethene is favored in the transition zone. A field site was selected where an aged pool exists at the bottom of a transition zone. Two boreholes were drilled to obtain sediment and groundwater samples to perform chemical, isotopic, molecular, and clone library analyses and microcosm experiments. The main results were as follows: (i) the transition zone is characterized by a high microbial richness; (ii) reductively dechlorinating microorganisms are present and partial reductive dechlorination coexists with denitrification, Fe and Mn reduction, and sulfate reduction; (iii) reductively dechlorinating microorganisms were also present in the zone of the aged pool; (v) the high concentrations of perchloroethene in this zone resulted in a decrease in microbial richness; (vi) however, the presence of fermenting microorganisms supplying electrons for the reductively dechlorinating microorganisms prevented the reductive dechlorination to be inhibited. These findings suggest that biostimulation and/or bioaugmentation could be applied to promote complete reductive dechlorination and to enhance the dissolution of more nonaqueous phase liquids (DNAPL).
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References
Adamson DT, Chapman S, Mahler N, Newell C, Parker BL, Pitkin S, Rossi M, Singletary M (2014) Membrane Interface probe protocol for contaminants in low-permeability zones. Ground Water 52(4):550–565
Aelion CM, Höhener P, Hunkeler D, Aravena R (Eds) (2009) Environmental isotopes in biodegradation and bioremediation. CRC Press
Aulenta F, Pera A, Rossetti S, Papini MP, Majone M (2007) Relevance of side reactions in anaerobic reductive dechlorination microcosms amended with different electron donors. Water Res 41(1):27–38
Azadpour-Keeley A, Keeley JW, Russell HH, Sewell GW (2001) Monitored natural attenuation of contaminants in the subsurface: processes. Groundwater Monit Rem 21(2):97–107
Bouwer EJ (1994) Bioremediation of chlorinated solvents using alternate electron acceptors. In: Norris RD et al (eds) Handbook of bioremediation. Lewis Publishers, p. 149–175
Bradley PM (2003) History and ecology of chloroethene biodegradation: a review. Biorem J 7:81–109
Bradley PM (2011) Reinterpreting the importance of oxygen based biodegradation in chloroethene contaminated groundwater. Ground Water Monit Rem 31(4):50–55
Bradley PM, Chapelle FH (2011) Microbial mineralization of dichloroethene and vinyl chloride under hypoxic conditions. Ground Water Monit Rem 31(4):39–49
Braeckevelt M, Fischer A, Kästner M (2012) Field applicability of compound-specific isotope analysis (CSIA) for characterization and quantification of in situ contaminant degradation in aquifers. Appl Microbiol Biotechnol: 1–21
Brookings DG (1988) Eh-Ph diagrams for geochemistry. Springer Verlag, New York
Chang YC, Hatsu M, Jung K, Yoo YS, Takamizawa K (2000) Isolation and characterization of a tetrachloroethylene dechlorinating bacterium, Clostridium bifermentans DPH-1. J Biosci Bioeng 89(5):489–491
Chang YC, Ikeutsu K, Toyama T, Choi D, Kikuchi S (2011) Isolation and characterization of tetrachloroethylene-and cis-1, 2-dichloroethylene-dechlorinating propionibacteria. J Ind Microbiol Biotechnol 38(10):1667–1677
Chapelle FH (1996) Quantifying rates of biodegradation in contaminated aquifers. In: Kobus H et al. (eds) Groundwater and subsurface remediation. Springer, Berlin Heidelberg, pp. 67–75
Chapman SW, Parker BL (2005) Plume persistence due to aquitard back diffusion following dense nonaqueous phase liquid source removal or isolation. Water Resour Res 41(12):W12411
Chapman SW, Parker BL, Cherry JA, Aravena R, Hunkeler D (2007) Groundwater-surface water interaction and its role on TCE groundwater plume attenuation. J Contam Hydrol 91(3):203–232
Chapman SW, Parker BL, Sale TC, Doner LA (2012) Testing high resolution numerical models for analysis of contaminant storage and release from low permeability zones. J Contam Hydrol 136:106–116
Cherry JA, Parker BL, Bradbury KR, Eaton TT, Gotkowitz MB, Hart DJ, Borchardt MA (2006) Contaminant transport through aquitards: a state-of-the-science review. American Water Works Association, AWWA (Ed.). Research Foundation, and International Water Well Association, IWA. Denver, Colorado, U.S.A.
Duhamel M, Edwards EA (2006) Microbial composition of chlorinated ethene-degrading cultures dominated by Dehalococcoides. FEMS Microbiol Ecol 58:538–549. doi:10.1111/j.1574-6941.2006.00191.x
Duhamel M, Mo K, Edwards EA (2004) Characterization of a highly enriched Dehalococcoides-containing culture that grows on vinyl chloride and trichloroethene. Appl Environ Microbiol 70:5538–5545. doi:10.1128/AEM.70.9.5538-5545.2004
Einarson MD, Cherry JA (2002) A new multilevel ground water monitoring system using multichannel tubing. Groundwater Monit Rem 22(4):52–65
Estrada-de Los Santos P, Vacaseydel-Aceves NB, Martínez-Aguilar L, Cruz-Hernández MA, Mendoza-Herrera A, Caballero-Mellado J (2011) Cupriavidus and Burkholderia species associated with agricultural plants that grow in alkaline soils. J Microbiol 49(6):867–876
Feenstra S, Mackay DC, Cherry JA (1991) A method assessing residual NAPL based on organic chemical concentrations in soil samples. Ground Water Monit Rev 1991:128–136
Fetter CW (1993) Contaminant hydrogeology. MacMillan Publishing Company, New York
Futamata H, Nagano Y, Watanabe K, Hiraishi A (2005) Unique kinetic properties of phenol-degrading variovorax strains responsible for efficient trichloroethylene degradation in a chemostat enrichment culture unique kinetic properties of phenol-degrading Variovorax strains responsible for efficient trichloro. Appl Environ Microbiol 71(2):904–911
Garrels RM, Christ CL (1965) Solutions, minerals and equilibria. Harper and Row, New York and John Weatherhill, Inc, Tokyo
Haack SK, Bekins BA (2000) Microbial populations in contaminant plumes. Hydrogeol J 8(1):63–76
Hartog H, Cho J, Parker BL, Annable MD (2010) Characterization of a heterogeneous DNAPL source zone in the Borden aquifer using partitioning and interfacial tracers: residual morphologies and background sorption. J Contam Hydrol 115(1):79–89
Humphries JA, Ashe AMH, Smiley JA, Johnston CG (2005) Microbial community structure and trichloroethylene degradation in groundwater. J Microbiol 51:433–439
Hunkeler D, Morasch B (2010) Isotope fractionation during transformation processes. In: Aelion CM, Höhener P, Hunkeler D, Aravena R (eds) Environmental isotopes in biodegradation and bioremediation. CRC Press, pp 79–125
Hunkeler D, Meckenstock R, Sherwood Lollar B, Schmidt T, Wilson T (2008) A guide for assessing biodegradation and source identification of organic ground water contaminants using compound specific isotope analysis (CSIA). Office of Research and Development, National Risk Management Research Laboratory, US Environmental Protection Agency
IGC (1996) Mapa Geològic de Catalunya 1:25.000. No. 258–1-2 (77–22): Navata. Institut Cartogràfic de Catalunya. Servei Geològic de Catalunya. Barcelona
IGME (1994) Mapa Geológico de España 1:50.000. No. 258: Figueres. Instituto Geológico y Minero de España, Madrid
Johnston D (2006) Draft EPA guidelines regulatory monitoring and testing groundwater sampling, 56, Environment Protection authority (EPA) Australia
Kim ES, Nomura I, Hasegawa Y, Takamizawa K (2006) Characterization of a newly isolatedcis-1, 2-dichloroethylene and aliphatic compound-degrading bacterium, clostridium sp. strain KYT-1. Biotechnol Bioprocess Eng 11:553–556
Lide DR (2003) Handbook of chemistry and physics, 84th edn. CRC Press Ltd., New York
Löffler FE, Sun Q, Li J, Tiedje JM (2000) 16S rRNA gene-based detection of tetrachloroethene-dechlorinating Desulfuromonas and Dehalococcoides species. Appl Environ Microbiol 66(4):1369–1374
Mackay D, Shiu WY, Ma KC, Lee SC (2006) Handbook of physical-chemical properties and environmental fate for organic chemicals. CRC press
Maymó-Gatell X, Chien Y, Gossett JM, Zinder SH (1997) Isolation of a bacterium that reductively dechlorinates tetrachloroethene to ethene. Science 276(5318):1568–1571
Maymó-Gatell X, Nijenhuis I, Zinder SH (2001) Reductive dechlorination of cis-1, 2-dichloroethene and vinyl chloride by “Dehalococcoides ethenogenes”. Environ Sci Technol 35(3):516–521
Men Y, Seth EC, Yi S, Allen RH, Taga ME, Alvarez-Cohen L (2014) Sustainable growth of Dehalococcoides mccartyi 195 by corrinoid salvaging and remodeling in defined lactate-fermenting consortia. Appl Environ Microbiol 80:2133–2141
Mercer JW, Cohen RM (1990) A review of immiscible fluids in the subsurface: properties, models, characterization and remediation. J Contam Hydrol 6(2):107–163
Miller E, Wohlfarth G, Diekert G (1996) Studies on tetrachloroethene respiration in Dehalospirillum multivorans. Arch Microbiol 166:379–387
Mukherjee P, Roy P (2012) Identification and characterisation of a bacterial isolate capable of growth on trichloroethylene as the sole carbon source. Adv Microbiol 02(03):284–294
National Research Council (1999) Improving management of persistent of contaminants. Groundwater and soil cleanup. National Academic Press, Washington, DC, pp. 113–174
Okeke BC, Chang YC, Hatsu M, Suzuki T, Takamizawa K (2001) Purification, cloning, and sequencing of an enzyme mediating the reductive dechlorination of tetrachloroethylene (PCE) from clostridium bifermentans DPH-1. Can J Microbiol 47(5):448–456
Olaniran AO, Pillay D, Pillay B (2008) Aerobic biodegradation of dichloroethenes by indigenous bacteria isolated from contaminated sites in Africa. Chemosphere 73(1):24–29
Park W, Lee S (2013) The biological degradation of high concentration of trichloroethylene (TCE) by Delftia acidovornas EK2. Korean J Microbiol 46
Parker BL, Gillham RW, Cherry JA (1994) Diffusive disappearance of immiscible phase organic liquids in fractured geologic media. Ground Water 32(5):805–820
Parker BL, Cherry JA, Chapman SW, Guilbeault MA (2003) Review and analysis of chlorinated solvent dense nonaqueous phase liquid distributions in five Sandy aquifers. Vadose Zone J 2:116–137
Parker BL, Cherry JA, Chapman SW (2004) Field study of TCE diffusion profiles below DNAPL to assess aquitard integrity. J Contam Hydrol 74(1):197–230
Parker BL, Chapman SW, Guilbeault MA (2008) Plume persistence caused by back diffusion from thin clay layers in a sand aquifer following TCE source-zone hydraulic isolation. J Contam Hydrol 102(1):86–104
Patil SS, Adetutu EM, Aburto-Medina A, Menz IR, Ball AS (2014) Biostimulation of indigenous communities for the successful dechlorination of tetrachloroethene (perchloroethylene)-contaminated groundwater. Biotechnol Lett 36(1):75–83
Puigserver D, Carmona JM, Cortés A, Viladevall M, Nieto JM, Grifoll M, Parker BL (2013) Subsoil heterogeneities controlling porewater contaminant mass and microbial diversity at a site with a complex pollution history. J Contam Hydrol 144(1):1–19
Puigserver D, Cortés A, Viladevall M, Nogueras X, Parker BL, Carmona JM (2014) Processes controlling the fate of chloroethenes emanating from DNAPL aged sources in river-aquifer contexts. J Contam Hydrol 168:25–40
Puigserver D, Nieto JM, Grifoll M, Vila J, Cortés A, Viladevall M, Parker BL, Carmona JM (2016) Temporal hydrochemical and microbial variations in microcosm experiments from sites contaminated with chloromethanes under biostimulation with lactic acid. Biorem J 20(1):54–70
Puls RW, Barcelona MJ (1996) Low-flow (minimal drawdown) ground-water sampling procedures. US Environmental Protection Agency, Office of Research and Development, Office of Solid Waste and Emergency Response. EPA Ground Water Issue
Rifai HS, Newell CJ, Wiedemeier TH (2011) Contamination cleanup: natural attenuation and advanced remediation technologies. Handbook of solvents. William Andrew, Toronto, pp. 1572–1630
Rivett MO, Dearden RA, Wealthall GP (2014) Architecture, persistence and dissolution of a 20 to 45 year old trichloroethene DNAPL source zone. J Contam Hydrol 170:95–115
Sale TC, Zimbron JA, Dandy DS (2008) Effects of reduced contaminant loading on downgradient water quality in an idealized two-layer granular porous media. J Contam Hydrol 102(1):72–85
Schaefer CE, Towne RM, Vainberg S, McCray JE, Steffan RJ (2010) Bioaugmentation for treatment of dense non-aqueous phase liquid in fractured sandstone blocks. Environ Sci Technol 44(1):4958–4964
Schlötelburg C, Wintzingerode C, Hauck R, Wintzingerode F, Hegemann W, Göbel UB (2002) Microbial structure of an anaerobic bioreactor population that continuously dechlorinates 1,2-dichloropropane. FEMS Microbiol Ecol 39:229–237. doi:10.1111/j.1574-6941.2002.tb00925.x
Sleep BE, Seepersad DJ, Mo K, Heidorn CM, Hrapovic L, Morrill PL, McMaster ML, Hood ED, LeBron C, Sherwood Lollar B, Major DW, Edwards EA (2006) Biological enhancement of tetrachloroethene dissolution and associated microbial community changes. Environ Sci Technol 40(11):3623–3633
Sung Y, Ritalahti KM, Sanford RA, Urbance JW, Flynn SJ, Tiedje JM, Löffler FE (2003) Characterization of two tetrachloroethene-reducing, acetate-oxidizing anaerobic bacteria and their description as Desulfuromonas michiganensis sp. nov. Appl Environ Microbiol 69(5):2964–2974
Tiehm A, Schmidt KR (2011) Sequential anaerobic/aerobic biodegradation of chloroethenes-aspects of field application. Curr Opin Biotechnol 22(3):415–421
Trevors JT (1996) Sterilization and inhibition of microbial activity in soil. J Microbiol Methods 26(1):53–59
USEPA (1998) Technical protocol for evaluating natural attenuation of chlorinated solvents in ground water. EPA/600/R-98/128. Office of Research and Development. Washington DC 20460
van der Zaan B, Hannes F, Hoekstra N, Rijnaarts H, de Vos WM, Smidt H, Gerritse J (2010) Correlation of Dehalococcoides 16S rRNA and chloroethene-reductive dehalogenase genes with geochemical conditions in chloroethene-contaminated groundwater. Appl Environ Microbiol 76(3):843–850
Verce MF, Gunsch CK, Danko AS, Freedman D (2002) Cometabolism of cis-1, 2-dichloroethene by aerobic cultures grown on vinyl chloride as the primary substrate. Environ Sci Technol 36:2171–2177
Vogel TM, Criddle CS, McCarty PL (1987) ES&T critical reviews: transformations of halogenated aliphatic compounds. Environ Sci Technol 21(8):722–736
Wei N, Finneran KT (2011) Influence of ferric iron on complete dechlorination of trichloroethylene (TCE) to ethene: Fe (III) reduction does not always inhibit complete dechlorination. Environ Sci Technol 45(17):7422–7430
Wiedemeier TH, Haas PE (2002) Designing monitoring programs to effectively evaluate the performance of natural attenuation. Ground Water Monit Rem 22(3):124–135
Wiedemeier TH, JT Wilson, JE Hansen, FH Chapelle, MA Swanson (1998) Technical protocol for evaluating natural attenuation of chlorinated solvents in groundwater. Air Force Center for Environmental Excellence Brooks AFB TX
Yang YR, McCarty PL (2000) Biologically enhanced dissolution of tetrachloroethene DNAPL. Environ Sci Technol 34(14):2979–2984
Yang YR, McCarty PL (2002) Comparison between donor substrates for biologically enhanced tetrachloroethene DNAPL dissolution. Environ Sci Technol 36(15):3400–3404
Yoshida N, Asahi K, Sakakibara Y, Miyake K, Katayama A (2007) Isolation and quantitative detection of tetrachloroethene (PCE)-dechlorinating bacteria in unsaturated subsurface soils contaminated with chloroethenes. J Biosci Bioeng 104(2):91–97
Acknowledgments
We are indebted to the Catalan Water Agency and to the members of INTERFREN of Figueres and INTECSON S.L. of Reus for their support and cooperation while conducting the fieldwork. We would also like to thank our colleagues of the Department of Geochemistry, Petrology, and Geological Prospecting of the University of Barcelona and especially the members of the hydrogeology group of that department. We are grateful to the Scientific-Technical Services personnel of the University of Barcelona for their help in analyzing the samples. We would also like to acknowledge the institution funding the research conducted within the following projects: CTM 2005-07824 and CGL 2008-02164/BTE (Spanish Ministry of Education).
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Puigserver, D., Herrero, J., Torres, M. et al. Reductive dechlorination in recalcitrant sources of chloroethenes in the transition zone between aquifers and aquitards. Environ Sci Pollut Res 23, 18724–18741 (2016). https://doi.org/10.1007/s11356-016-7068-4
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DOI: https://doi.org/10.1007/s11356-016-7068-4